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Origin and Potential Expansion of the Invasive Longan Lanternfly

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Origin and Potential Expansion of the Invasive Longan Lanternfly biology Article Origin and Potential Expansion of the Invasive Longan Lanternfly, Pyrops candelaria (Hemiptera: Fulgoridae) in Taiwan You-Sheng Lin, Jhih-Rong Liao * , Shiuh-Feng Shiao * and Chiun-Cheng Ko † Department of Entomology, National Taiwan University, Taipei City 106332, Taiwan; [email protected] (Y.-S.L.); [email protected] (C.-C.K.) * Correspondence: [email protected] (J.-R.L.); [email protected] (S.-F.S.) † Deceased, 29 October 2020 this paper is dedicated to the memory of late Chiun-Cheng Ko. Simple Summary: The longan lanternfly Pyrops candelaria (Linnaeus), which feeds on longan trees, has invaded the main island of Taiwan. Thus, this study aimed to (1) trace the origin of invasion, (2) predict habitat suitability and (3) study the risk of lanternfly spread into crop cultivation areas. We reconstructed the longan lanternfly phylogeny to compare haplotypes among different regions. In addition, we predicted the habitat suitability for the species based on MaxEnt and then matched it with longan and pomelo cultivation areas. Our results indicated that the Taiwanese populations of longan lanternfly might originate from the Kinmen Islands and the plain areas of Taiwan are considered to have high habitat suitability. Abstract: The longan lanternfly Pyrops candelaria is a new invasive species on the main island of Taiwan. The introduction of an invasive species may negatively influence the native fauna, flora and environment. Thus, this study aimed to infer the invasion history, predict habitat suitability and Citation: Lin, Y.-S.; Liao, J.-R.; Shiao, potential expansion and assess the risk to crop cultivation areas in Taiwan. Genetic structures of P. S.-F.; Ko, C.-C. Origin and Potential candelaria from the main island of Taiwan and related regions were analyzed based on partial COI Expansion of the Invasive Longan and ND2 sequences. Additionally, machine learning MaxEnt was utilized to study habitat suitability. Lanternfly, Pyrops candelaria The results suggested that the Taiwanese populations may originate from the Kinmen Islands and (Hemiptera: Fulgoridae) in Taiwan. the plain areas of Taiwan are considered to have high habitat suitability. Furthermore, most of the Biology 2021, 10, 678. https:// cultivation areas of longan and pomelo crops showed high habitat suitability. doi.org/10.3390/biology10070678 Keywords: genetic structure; biological invasion; Pyrops candelaria; longan lanternfly; habitat suitability Academic Editor: Klaus H. Hoffmann Received: 21 June 2021 Accepted: 15 July 2021 1. Introduction Published: 17 July 2021 Biological invasions may pose threats to native fauna and flora, the economy and even Publisher’s Note: MDPI stays neutral human health [1], constituting a global economic and ecological threat [2–4]. Numerous with regard to jurisdictional claims in human activities (e.g., international trade and travel) have enabled certain species to cross published maps and institutional affil- their natural geographical barriers to invade a new region [4–6]. Understanding the genetic iations. structures of invasive species is helpful for effective management and quarantine [7–9]. The mitochondrial cytochrome oxidase subunit I (COI) and NADH dehydrogenase subunit 2 (ND2) genes have been used in studies of genetic structures (e.g., Tessaratoma papillosa (Drury) and Lycorma delicatula (White)) [7,8]. Moreover, the maximum entropy method (MaxEnt), a machine learning approach, has been widely used to explore species niches by Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. analyzing species-environment relationships using presence-only data and environmental This article is an open access article variables [10]. As only presence data are required, this method has multiple applications, distributed under the terms and including determining suitable habitats for protected species [10], predicting the distribu- conditions of the Creative Commons tion of invasive species [11], studying the establishment of invasive natural enemies [12] Attribution (CC BY) license (https:// and modeling distribution shifts caused by climatic changes [13]. creativecommons.org/licenses/by/ Hobbyists aspire to obtain live lanternfly specimens because of their fascinating 4.0/). appearance and scarcity in the market; however, certain lanternfly species could become Biology 2021, 10, 678. https://doi.org/10.3390/biology10070678 https://www.mdpi.com/journal/biology Biology 2021, 10, 678 2 of 13 serious pests. For instance, the spotted lanternfly (Lycorma delicatula) is a notoriously invasive species that causes great economic losses to the grape industry [6]. The longan lanternfly Pyrops candelaria (Linnaeus) (Hemiptera: Fulgoridae) is a large species with an exaggerated cephalic process and magnificent wing pattern (Figure1), making it popular among collectors. This species is distributed in China, India, Myanmar, Thailand, Vietnam, Cambodia, Indonesia (Java) and Kinmen, an outlying island of Taiwan (Figure2)[14–17] . The major host plants of the longan lanternfly are longan (Dimocarpus longan Lour.), pomelo (Citrus maxima Merr.) and mango (Mangifera indica Linnaeus) [18]. This species was observed for the first time in Wugu and Bali in Northern Taiwan in 2018. On Kinmen Islands, the longan lanternfly is regarded as a mascot. The remarkable appearance renders the species an excellent subject for environmental education. The insect also attracts many wildlife photographers from the main island to Kinmen every year. In addition, the Kinmen Islands are the nearest native region for the longan lanternfly without tight quarantine, since it belongs to the territory of Taiwan. As a result, Kinmen Islands are a possible origin of invasion. Previous studies have reported the longan lanternfly as an agricultural pest [15,19,20], but no significant impact has been observed since its invasion. Nevertheless, the ecological effects of invasive species are unpredictable. Therefore, from the conservation perspective, management of the longan lanternfly should be taken seriously. This study aimed to trace the invasion history of the longan lanternfly, predict the potential expansion area and assess the risk to crop cultivation areas in Taiwan. First, we hypothesized that the origin of invasion is Kinmen Islands; therefore, genetic structures for the newly introduced populations of P. candelaria were reconstructed and the haplotypes among different regions were compared. Second, MaxEnt was used to predict the potential distribution of P. candelaria in Taiwan with inferences drawn for habitat suitability under certain climatic conditions, including temperature and precipitation. Finally, the potential distribution areas were matched with information on the host plant cultivation areas. Biology 2021, 10, x FOR PEER REVIEW 3 of 14 The result is a combination of climatic factors and host plant information to improve the credibility of risk assessment for invasion and potential spread. Figure 1. AdultAdult individuals individuals of of the the longan longan lanternfly, lanternfly, Pyrops candelaria (Linnaeus) on its main host plant, Dimocarpus longan . Figure 2. Global occurrence of Pyrops candelaria. The triangles represent distribution records. Biology 2021, 10, x FOR PEER REVIEW 3 of 14 Biology 2021, 10, 678 3 of 13 Figure 1. Adult individuals of the longan lanternfly, Pyrops candelaria (Linnaeus) on its main host plant, Dimocarpus longan. Figure 2. Global occurrence of Pyrops candelaria. The triangles represent distribution records. 2. Materials and Methods 2.1. Genetic Structure and Phylogenetic Reconstruction of P. candelaria in Taiwan and Related Regions 2.1.1. Sample Preparation, PCR Amplification and Sequencing A total of 155 P. candelaria specimens were collected from the main island of Taiwan (n = 105) and several native regions, including China (n = 5), Thailand (n = 20), Hong Kong (n = 3), Macau (n = 1), Kinmen (n = 20) and Matsu (n = 1) (Table S1). All samples were preserved in 95% ethanol and stored at −20 ◦C. Genomic DNA was extracted from the single tarsi of P. candelaria specimens using QuickExtract™ DNA Extraction Solution 1.0 (Epicenter) according to the manufacturer’s protocol for insect tissue. Two partial sequences from the mitochondrial cytochrome oxidase subunit I (COI) and NADH dehydrogenase 2 (ND2) genes were targeted for amplification. The COI gene was amplified using the universal primers LCO1490 (50- GGTCAACAAATCATAAAGATATTGG-30) and HCO2198 (50-TAAACTTCAGGGTGACCA AAAAATCA-30)[21] and the ND2 gene was amplified using primers ND2-41F (50-ATGACA ATAAGAGTAATAAT-30) and ND2-819R (50-TGAAATTAATGATGATCTGA-30), which were designed in this study. The reaction mixture contained 2 µL of extracted DNA, 0.5 µL ® of each primer, 4 µL of 5× FIREPol Master Mix (Solis BioDyne) and 13 µL of ddH2O. The PCR included an initial denaturation at 94 ◦C for 2 min, followed by 35 cycles of 30 s denaturation at 94 ◦C, 30 s annealing at 47.5 ◦C and 40 ◦C for the COI and ND2 genes, respectively, 45 s extension at 72 ◦C and a final extension at 72 ◦C for 10 min. Automatic sequencing was performed using an ABI 3730XL DNA Analyzer (Applied Biosystems). 2.1.2. Sequence Analyses and Phylogenetic Reconstruction Sequences were edited and assembled into contiguous sequences using BioEdit 7.0.5.3 [22] and sequence alignments were performed automatically using the MAFFT 7.0 online server [23]. Haplotype network analysis was applied using TCS 1.21 [24] and modified using tcsBU [25]. Pairwise genetic distances between different populations were estimated using
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